Vestibular modulation of somatosensory perception

Functional imaging studies show that vestibular and somatosensory projections overlap in the human brain. However, it remains unclear whether and how vestibular inputs affect somatosensory function. To address this issue, we studied the effects of left caloric vestibular stimulation (CVS) on detection of near‐threshold somatosensory stimuli delivered to the left and right hands of healthy volunteers. To investigate whether these effects were somatosensory specific, or supramodal, we also tested CVS modulation of visual contrast detection. Signal detection analyses showed increased somatosensory perceptual sensitivity immediately after CVS, both ipsilaterally and contralaterally. No statistically reliable effects on visual contrast sensitivity were found. These findings suggest that vestibular stimulation has a specific facilitatory effect on somatosensory detection, distinct from non‐specific arousal and spatial attentional effects of CVS. Thus, the overlap in brain activations for vestibular and somatosensory inputs is not simply an anatomical curiosity, but may reflect a functional cross‐modal perceptual interaction.

[1]  O. Grüsser,et al.  Vestibular neurones in the parieto‐insular cortex of monkeys (Macaca fascicularis): visual and neck receptor responses. , 1990, The Journal of physiology.

[2]  T. Brandt,et al.  Reciprocal inhibitory visual-vestibular interaction. Visual motion stimulation deactivates the parieto-insular vestibular cortex. , 1998, Brain : a journal of neurology.

[3]  A Weindl,et al.  Deactivation of human visual cortex during involuntary ocular oscillations. A PET activation study. , 1996, Brain : a journal of neurology.

[4]  O. Blanke,et al.  Neural Basis of Embodiment: Distinct Contributions of Temporoparietal Junction and Extrastriate Body Area , 2006, The Journal of Neuroscience.

[5]  Richard S. J. Frackowiak,et al.  Identification of the central vestibular projections in man: a positron emission tomography activation study , 2004, Experimental Brain Research.

[6]  H. Levitt Transformed up-down methods in psychoacoustics. , 1971, The Journal of the Acoustical Society of America.

[7]  D. Wolpert,et al.  Sensorimotor attenuation by central motor command signals in the absence of movement , 2006, Nature Neuroscience.

[8]  R. Sterzi,et al.  Exploring somatosensory hemineglect by vestibular stimulation. , 1993, Brain : a journal of neurology.

[9]  G. Bottini,et al.  How the vestibular system modulates tactile perception in normal subjects: a behavioural and physiological study , 2011, Experimental Brain Research.

[10]  J. Driver,et al.  Do neck-proprioceptive and caloric-vestibular stimulation influence covert visual attention in normals, as they influence visual neglect? , 2001, Neuropsychologia.

[11]  D. O'connell,et al.  A CONCENTRIC SHOCK ELECTRODE FOR PAIN STIMULATION. , 1965, Psychophysiology.

[12]  Steven Mark Miller,et al.  The changing face of perceptual rivalry , 2008, Brain Research Bulletin.

[13]  François Klam,et al.  ã Federation of European Neuroscience Societies Visual±vestibular interactive responses in the macaque ventral intraparietal area (VIP) , 2022 .

[14]  G. Curio,et al.  Imperceptible Stimuli and Sensory Processing Impediment , 2003, Science.

[15]  K. Utz,et al.  A long-lasting improvement of tactile extinction after galvanic vestibular stimulation: Two Sham-stimulation controlled case studies , 2011, Neuropsychologia.

[16]  S. Cappa,et al.  Temporary Remission of Left Hemianesthesia after Vestibular Stimulation. A Sensory Neglect Phenomenon , 1990, Cortex.

[17]  J. Paysant,et al.  Vestibular caloric stimulation evokes phantom limb illusions in patients with paraplegia , 2001, Spinal Cord.

[18]  M. Bach,et al.  The Freiburg Visual Acuity test--automatic measurement of visual acuity. , 1996, Optometry and vision science : official publication of the American Academy of Optometry.

[19]  Y. Lacasse,et al.  From the authors , 2005, European Respiratory Journal.

[20]  Hidenao Fukuyama,et al.  Cortical correlates of vestibulo-ocular reflex modulation: a PET study. , 2003, Brain : a journal of neurology.

[21]  A. Iriki,et al.  Bilateral hand representation in the postcentral somatosensory cortex , 1994, Nature.

[22]  Rüdiger Wenzel,et al.  Human Vestibular Cortex as Identified with Caloric Stimulation in Functional Magnetic Resonance Imaging , 2002, NeuroImage.

[23]  H. Kornhuber Zur Bedeutung multisensorischer Integration im Nervensystem , 1965, Deutsche Zeitschrift für Nervenheilkunde.

[24]  J. M. Fredrickson,et al.  Projection of the vestibular nerve to the area 3a arm field in the squirrel monkey (Saimiri Sciureus) , 2004, Experimental Brain Research.

[25]  Richard C Fitzpatrick,et al.  Virtual head rotation reveals a process of route reconstruction from human vestibular signals , 2005, The Journal of physiology.

[26]  J. Paysant,et al.  Temporary phantom limbs evoked by vestibular caloric stimulation in amputees. , 2001, Neuropsychiatry, neuropsychology, and behavioral neurology.

[27]  Richard S. J. Frackowiak,et al.  Modulation of conscious experience by peripheral sensory stimuli , 1995, Nature.

[28]  Stephan Riek,et al.  Interhemispheric switching mediates perceptual rivalry , 2000, Current Biology.

[29]  A. Rubens Caloric stimulation and unilateral visual neglect , 1985, Neurology.

[30]  N. Forss,et al.  Functional characterization of human second somatosensory cortex by magnetoencephalography , 2002, Behavioural Brain Research.

[31]  F Fazio,et al.  Left caloric vestibular stimulation ameliorates right hemianesthesia , 2005, Neurology.

[32]  J. Duhamel,et al.  Multisensory Integration in the Ventral Intraparietal Area of the Macaque Monkey , 2007, The Journal of Neuroscience.

[33]  D. Angelaki,et al.  Vestibular system: the many facets of a multimodal sense. , 2008, Annual review of neuroscience.

[34]  E. Macaluso,et al.  Multisensory spatial interactions: a window onto functional integration in the human brain , 2005, Trends in Neurosciences.

[35]  Steven Mark Miller,et al.  Caloric vestibular stimulation reveals discrete neural mechanisms for coherence rivalry and eye rivalry: A meta-rivalry model , 2007, Vision Research.

[36]  E. Bisiach,et al.  Remission of somatoparaphrenic delusion through vestibular stimulation , 1991, Neuropsychologia.

[37]  E. Bisiach,et al.  Remission of hemineglect and anosognosia during vestibular stimulation , 1987, Neuropsychologia.

[38]  Hans-Otto Karnath,et al.  Neglect-like behavior in healthy subjects , 2003, Experimental Brain Research.

[39]  Sidney S. Simon,et al.  Merging of the Senses , 2008, Front. Neurosci..

[40]  S. Faugier-Grimaud,et al.  Anatomic connections of inferior parietal cortex (area 7) with subcortical structures related to vestibulo‐ocular function in a monkey (macaca fascicularis) , 1989, The Journal of comparative neurology.

[41]  D. Schwarz,et al.  Rhesus Monkey Vestibular Cortex: A Bimodal Primary Projection Field , 1971, Science.

[42]  O J Grüsser,et al.  Localization and responses of neurones in the parieto‐insular vestibular cortex of awake monkeys (Macaca fascicularis). , 1990, The Journal of physiology.

[43]  T. Brandt,et al.  Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). , 2001, Journal of neurophysiology.